J. Hattori Bot. Lab. No. 76: 147- 157 (Oct. 1994)

POPULATION GENETICS OF BRYOPHYTES IN RELATION TO THEIR REPRODUCTIVE BIOLOGY

ROBERT WYATT1

ABSTRACT. Several unusual features of bryophyte reproduction lead to predictions about levels of genetic variation and its partitioning among natural populations. Dominance of the life cycle by a free-living, haploid gametophyte suggests that levels of genetic variation should be low. lsozyme data indicate, however, that display a range of variation comparable to that observed for diploid . The range for liverworts is less. Because of the tight coupling of ploidy level and sexuality in most bryophytes, it is difficult to determine if levels of genetic variation are higher in unisexual than in bisexual taxa. Bisexual allopolyploids in and Rhizomnium typically show fixed heterozygosity, which inflates their gene diversity statistics relative to their unisexual, haploid congeners. Nevertheless, gene diversities are also higher for bisexual, haploid species of Plagiothecium than for their unisexual, haploid relatives. There are also few data available to test the prediction of higher rates of self-fertilization and greater differentiation among populations of bisexual than of unisexual mosses and liverworts. Restricted gene flow due to short sperm dispersal distances should lead to strong differentiation among populations, but this may be counteracted by long-distance dispersal of spores. Typically degrees of genetic differentiation among conspecific populations of bryophytes are similiar to those observed in seed plants, except that intercontinentally disj unct populations of bryophytes often are only weakly differentiated. Asexual reproduction is common and widespread in bryophytes and appears to lead to large clonal patches in some taxa. The recent discovery of several allopolyploid bryophytes suggests that interspecific hybridization is more common than has been thought. This conclusion fits better with the limited possibilities of bryophytes with respect to reproductive isolation, given that fertilization is external and effected by water in all taxa.

INTRODUCTION Reproduction in bryophytes is most similar to the situation prevailing in the pteridophytes. The most salient features include: ( 1) sexual reproduction is accom­ plished by free-living gametophytes; (2) fertilization is effected by motile sperms that are released into free water; (3) intragametophytic self-fertilization is possible in species with bisexual gametophytes; ( 4) spores are typically small and may be carried long distances by the wind; and (5) asexual reproduction is widespread and common. The ferns and fern allies share all of these features with mosses, liverworts, and hornworts. The major differences between these two groups of land plants flow from the fact that the sporophyte generation is relatively reduced in size and importance in the bryophyte life cycle. Thus, most of the asexual processes in pteridophytes involve propagation of sporophytes. Another important distinction is that, whereas most pteridophytes are potentially bisexual, 60-70% of all bryophytes are unisexual (Wyatt and Anderson 1984). 1 Institute of Ecology, University of Georgia, Athens, Georgia 30602, U.S.A. 148 J. Hattori Bot. Lab. No. 76 I 9 9 4

PREDICTIONS Given the characteristic features of bryophyte reproduction, it is possible to predict their effect on the population genetics of these plants. ( l) Natural selection, acting directly on the haploid genotype of bryophyte gametophytes, should lead to reduced levels of genetic variation. Because new genetic variants that arise by mutation are immediately expressed, natural selection should eliminate them very quickly, even if they are only mildly deleterious. Unlike diploid plants and animals, in which deleterious alleles can be sheltered in the heterozygous state, all genetic variants within haploid gametophytes are exposed. Among others, Mulcahy ( 1979) has argued that intense selection on gametophytes of angiosperms (i.e., pollen tubes) has been of primary importance in the rise of the flowering plants to dominance. Szweykowski ( 1984) has pointed out that bryophyte populations should be likened to arrays of gametes in other land plants and has suggested that some unusual properties of and liverwort populations may derive from their unique structure. There are some basic differences of opinion regarding the base number of chromo­ somes for mosses and liverworts and, therefore, whether the genomes of gametophytic plants are truly haploid. Schuster ( 1966) and Newton (1983) believe that modern liverworts are ancient polyploids built up from a base number of x = 4 or 5. On the other hand, Smith (1978) and Crosby ( 1980) contend that the base number is x = 8- 10. For most mosses it seems likely that the base number is x = 6 or 7 (Smith 1978; Anderson 1980). This is consistent with all isozyme studies to date, which have reported simple haploid patterns of expression in taxa at the presumed base level. Thus, it appears that arguments predicated on natural selection acting on functionally haploid genotypes in bryophytes are appropriate for these taxa. (2) Some mosses and liverworts are capable of producing bisexual gametophytes. This creates a situation in which there are three possibilities with respect to mating: ( l) there can be intergametophytic crossing, cross-fertilization of gametophytes produced by different sporophytes, which is analogous to outcrossing in seed plants; (2) there can be intergametophytic selfing, cross-fertilization of gametophytes produced by the same sporophyte, which is analogous to selfing in seed plants; and (3) there can be intragametophytic selfing, self-fertilization of a single gametophyte, which is a mating possibility unique to bryophytes and homosporous pteridophytes and which results in a diploid sporophyte that is homozygous at all loci. In most bryophytes, however, this third possibility is eliminated by unisexuality. According to Wyatt and Anderson ( 1984 ), approximately 60% of mosses and 70% of liverworts are unisexual, and even among bisexual species there may be mechanisms that favor cross-fertilization between gametophytes. Nevertheless, to the extent that self-fertilization does occur more frequently in bisexual than in unisexual mosses and liverworts, we can predict higher rates of inbreeding. This, in turn, should result in significant genetic substructuring of popula­ tions. Moreover, inbreeding species should partition relatively more of their genetic variation among, rather than within, populations. There should be greater potential for R. WYATT: Population genetics of bryophytes in relation to their reproductive biology 149 racial differentiation across the species range. (3) Gene flow in bryophytes is effected during sexual reproduction by dispersal of sperms and of spores. All recent reviews of sperm dispersal in mosses and liverworts have reached the same conclusion: sperm dispersal distances are very short (Wyatt & Anderson 1983). Even in larger species with splash cups, only rarely do sperms get dispersed more than 50cm. In species without splash cups, fertilization typically occurs within a radius of about 10 cm. Many authors have assumed that the spores of bryophytes are capable of long­ distance transport by the wind. It is certainly true that many moss and liverwort species are very widely distributed. Detailed studies attempting to quantify spore dispersal from natural populations, however, have documented that deposition declines pre­ cipitously as a function of distance from the source (Miles & Longton 1990, 1992; Stoneburner et al. 1992). Nevertheless, spores are produced in prodigious numbers and typically only a small fraction are trapped; thus, it is possible that many escape and travel long distances to establish new colonies remote from the source. To the extent that gene flow, presumably almost entirely by spores or asexual fragments, is extensive between populations of bryophytes, we should expect popula­ tions to be relatively homogeneous across their ranges. If effective gene flow is more restricted, we predict that populations will be more strongly differentiated. If gene flow is very strongly limited, we might even expect to find genetic substructuring within populations from a single site. ( 4) In addition to the many and diverse forms of specialized asexual propagules, it appears that most, if not all, bryophytes are capable of asexual reproduction by regeneration of unspecialized fragments of the gametophytic thallus. In many cases it appears that asexual progagules are resistant to the perils of long-distance transport and may be carried great distances. On the other hand, they probably are also very important in increasing local poplation size (Wyatt 1982). To the extent that local populations of bryophytes increase in size by recruitment of clonal individuals, we should expect overall gene diversity to decrease. This would be especially true if certain genotypes were more successful than others at asexual reproduction. Over time local populations might come to be dominated by one or a few highly successful genotypes. On a larger scale, asexual reproduction would have much the same effect as inbreeding: enhancing levels of genetic differentation among popula­ tions across the species range. This effect might be counteracted, however, if asexual propagules were highly dispersible and tended to increase rates of gene flow between populations. (5) Unlike seed plants, which have various contrivances to effect delivery of sperms to eggs, bryophyte and pteridophyte sperms are released from antheridia to swim in free water using their flagella. Such unspecialized means of sperm delivery would appear to open wide the possibility of interspecific hybridization. Whenever the gametophytes of two species occur in the same place and mature at the same time, it would seem likely that sperms of one species might encounter and fertilize eggs of the other. Mixed-species stands of congeneric bryophytes are relatively common (e.g., 150 J. Hattori Bot. Lab. No. 76 I 9 9 4

Wyatt et al. 1982), and most mosses and liverworts in a given habitat show phenologies that are attuned to that habitat (e.g., Stark 1983). (6) In bryophytes, there is a clear correlation between and sexuality. Wyatt ( 1982) showed that haploid mosses and liverworts tend to be unisexual, whereas polyploid taxa tend to be bisexual. There are a number of celebrated cases in which a single polyploid member of a given clade is bisexual, whereas all of its close haploid relatives are unisexual (e.g., Lowry 1948, 1954; Yano 1957a, 1957b; Schuster 1966; Koponen & Nilsson 1977; Wyatt 1985). We might, therefore, predict that the genetic consequences of polyploidy in bryophytes, at least with respect to breeding systems, will be indentical to those associated with bisexuality. Polyploidy should lead to higher rates of inbreeding and greater levels of genetic differentiation between populations. Counteracting this trend to some extent, however, is the fact that polyploidy provides more raw material for mutation and allows the possibility of heterozygosity in the dominant gametophyte generation of the life cycle. Of course, tetrasomic inheritance in the sporophyte generation will tend to slow the action of natural selection. It is, therefore, difficult to predict precisely what the overriding effect of polyploidy will be in any given species of moss or liverwort.

EMPIRICAL EVIDENCE Recent reviews of the growing database on electrophoretically detectable genetic variation in mosses have concluded that the range of means for parameters such as percentage of loci polymorphic per population, alleles per locus, and expected hetero­ zygosity is similar to that reported for diploid vascular plants (Wyatt et al. 1989; Stoneburner et al. 1991). For example, within section Rosu la ta of Plagiomnium, P. ellipticum is polymorphic (i.e., expresses more than one allele) at 73.9% of the 23 loci scored. Mean number of alleles per locus is 2.4 ± 0.3 (mean ± standard error), and mean expected heterozygosity is 0.143 ± 0.043. These values are all on the high side of the range of means reported for vascular plants by Hamrick and Godt (1990). In contrast, data for P. insigne, another species in Plagiomnium section Rosulata, place it on the low side of the range of means. For P. insigne, 34.8% of the 23 loci are polymorphic, there are 1.5 ± 0.2 alleles per locus, and mean expected heterozygosity is 0.057 ± 0.030. Other moss species may have higher or lower levels of genetic variation. Neverthe­ less, the ultimate conclusion is that mosses maintain more genetic variation than would be predicted for organisms with a haploid-dominant life cycle. The explanation for this is not clear. Some authors have suggested that high levels of genetic variation in haploid organisms proves that isozyme polymorphisms are selectively neutral (Yamazaki 1981, 1984). On the other hand, Szweykowksi (1984) and Wyatt et al. (1989) have suggested scenarios under which at least some of this variation might be maintained by balancing selection. Of the hepatics studied thus far, it appears that levels of genetic variation are typically lower than for mosses (Wyatt et al. 1989; Stoneburner et al. 1991). Neverthe- R. WYA TT : Population genetics of bryophytes in relation to their reproductive biology 151 less, the levels are still higher than expected for haploid-dominant organisms. Levels of genetic variation are low in liverworts from glaciated portions of Europe. Wachowiak (1986), for example, found no electrophoretically dectectable variation in Plagiochila porel/oides. On the other hand, Dewey ( 1989) found that populations of Riccia dictyospora from granite outcrops in the southeastern United States are polymorphic at 20% of their loci, have 1.24 alleles per locus, and expected heterozygosity of 0.076. It is difficult to test the prediction that unisexual bryophytes should maintain more genetic variation than bisexual species, because of the close association between ploidy level and sexuality. For example, statistics of genetic diversity for bisexual Plagio­ mnium medium are higher than for its unisexual relatives (Wyatt et al. 1992). These statistics are misleading in this case, however, as it is known that P. medium is an allopolyploid (Wyatt et al. 1988). Thus, much of its apparent variation is actually due to fixed heterozygosity, resulting from nonsegregation of nonhomologous chromo­ somes. For a rigorous test of the prediction, it will be necessary to compare congeneric species that differ in sexuality but not in ploidy level, especially if the polyploid is of hybrid origin. Ideal material for such a test would come from comparisons of populations of plants such as Rhizomnium magnifolium, which is normally unisexual but exists as a bisexual "race" in Japan (Koponen 1973). It might also prove instructive to compare sister species that differ in sexuality, but not chromosome number, in such genera as Sphagnum, Bryum, Hypnum, and Thuidium. Hofman ( 1988) compared isoploid species of Plagiothecium that differed in sexuality and concluded that all measures of genetic variation were higher for bisexual than for unisexual species. She speculated, however, that effects of sexuality "might be obscured by differences between the species in the amount of asexual reproduction." It is also difficult to test unequivocally the prediction that higher rates of selfing in bisexual mosses and liverworts should lead to greater differentiation among popula­ tions. Indeed, it is not entirely clear that self-fertilization is the predominant mode of sexual reproduction in such species (Wyatt et al. 1989). Zielinski (1986) found that in the bisexual haploid liverwort Pellia epiphyl/a, at least 25 % of the sporophytes produced were the result of cross-fertilization. Similarly, Wyatt et al. (1988, 1992) argued that the large number of multilocus genotypes detected in the bisexual, allopolyploid moss Plagiomnium medium suggests that cross-fertilization is probably common. Nei's ( 1973) gene diversity statistics provide a useful way to compare partitioning of total diversity (HT) into that existing within (Hs) versus among populations (DsT ). The ratio of among to total variation ( G sT ) can be used as an indicator of how strongly differentiated populations of species are from one another. Within Plagiomnium section Rosulata, the bisexual P. medium has a relatively low G sT compared to the five unisexual species in the group (Wyatt 1992). Comparing P. medium to P. e//ipticum, which also has a broad circumboreal range, the former expresses only 12.8% of the total variation among populations, whereas the latter shows 36.0%. Similarly, the G sT value for bisexual Rhizomnium pseudopunctatum is exceptionally low (0.0452: Wyatt et 152 J. Hattori Bot. Lab. No. 76 I 9 9 4 al. 1993b). Thus, based on limited data, it appears that bisexual mosses are not more strongly differentiated across their ranges than are unisexual species. Gene flow is generally regarded as the most important factor in determining the degree of differentiation among populations of a species. In bryophytes it is clear that the potential dispersal distances of sperms are very short. The role of spore dispersal is more controversial (e.g., Wyatt 1982; Longton & Miles 1982; Longton & Schuster 1983; Mishler 1988; Miles & Longton 1990). Potentially, it would appear that the small, light spores of mosses and liverworts, which are produced in prodigious numbers, could regularly be carried great distances by the wind (Zanten 1976, 1978, 1984; Zanten & Gradstein 1988). This is so, even if most end up falling close to the source and/or fail to germinate and establish new colonies (Stoneburner et al. 1992; Miles & Longton 1992). The most commonly used measure of the degree of genetic differentiation between populations is Nei's ( 1972) genetic identity (I). For most mosses and liverworts, within-species values are similar to those reported for vascular plants (Wyatt et al. 1989; Stoneburner et al. 1991). For example, Plagiomnium ellipticum has a mean J = 0.946 and for Polytrichum commune, I = 0.933, values clearly within the range and only slightly below the mean reported by Gottlieb (1981) for 14 species of outcrossing flowering plants (/= 0.956). Similarly, Dewey's (1989) values for conspecific popula­ tions of three sibling species of the liverwort Riccia dictyospora ranged from 0.856 to 0.939. It would appear, therefore, that gene flow, presumably principally via spore dispersal, between populations of mosses and liverworts is sufficient to keep levels of genetic differentiation within the same range observed in vascular plants. There is a striking difference, however, between mosses and vascular land plants with respect to genetic differentiation at the largest scale. Intercontinentally disjunct populations of bryophytes are often treated as conspecific, whereas those of seed plants are typically considered congeneric species pairs. For Plagiomnium ellipticum and P. medium, Nei's (1972) genetic identities between European and North American populations were all > 0.85 (Wyatt et al. 1992). For Rhizomnium magnifolium and R. pseudopunctatum, genetic identities between European and North American popula­ tions were all > 0.92 (Wyatt et al. 1993b). Hofman (1990) also reported unexpectedly high genetic identities between intercontinentally disjunct populations of several species of Plagiothecium. In the liverwort Conocephalum conicum, Odrzykoski and Szweyko­ wski (1991) found mean genetic identities > 0.92 between European and North American populations of"species S." In contrast, Parks and Wendel (1990) reported a mean / = 0.43, ranging to a low of 0.32, between the North American Liriodendron tulipifera and the east Asian L. chinense. Similarly, Hoey and Parks ( 1991) reported genetic identities in the range 0.26-0. 51 between intercontinentally disjunct species of Liriodendron. Crawford et al. 's ( 1992) review of vascular species disjunctions concluded that intercontinentally disjunct species are typically very strongly differenti­ ated electrophoretically. Only in isolated instances of recent long-distance dispersal are the disjunct taxa similar isozymically. This explanation seems unlikely to apply in all of the cases involving bryophytes. It is, therefore, enigmatic why intercontinentally R. Wv A TT: Population genetics of bryophytes in relation to thei r reproductive biology 153 disjunct populations of mosses and liverworts show so little divergence relative to vascular plants (Wyatt et al. 1992). On a microgeographic scale, we can predict that bryophytes that regularly reproduce by asexual means should develop pronounced local population structure. Cummins and Wyatt ( 1981) detected genetic variation within contiguous patches (5 X 5 cm) of the moss Atrichum angustatum. Genetic polymorphism was also observed on this scale within patches of Plagiomnium ciliare by Wyatt et al. (1989). In these cases, at least, clones resulting from asexual reproduction are not always apparent. Innes ( 1990) found strong microgeographic differentiation among 16 subpopulations of a population of Polytrichumjuniperinum, but there was little variation within subpopula­ tions. A similar pattern was seen in Climacium americanum (Meagher & Shaw 1990) . Of 38 multilocus genotypes detected in Polytrichum commune, the mean number per population (3.9: Derda & Wyatt 1990) was much lower than for asexually reproducing diploid plants ( 16.1: Ellstrand & Roose 1987). Perhaps the most thorough study of microgeographic differentiation in a moss is that of Plagiothecium undulatum by Hofman ( 1990). She found that in subpopulations with frequent sexual reproduction, genotypes were essentially distributed at random. In subpopulations where asexual reproduction dominated, however, large colonal patches developed, as reflected in statistics showing local clumping of particular multilocus genotypes. The fact that bryophytes are characterized by a very crude and unspecialized mode of sperm delivery would seem to open up many possibilities for interspecific cross­ fertilization, just as in pteridophytes. Surprisingly, however, there are very few cases reported of interspecific hybrids in mosses or liverworts. Most reported hybrids involve wide crosses between genera of mosses that differ strikingly in sporophytic characters (Wyatt & Anderson 1984). These intergeneric hybrids usually produce only inviable spores and, hence, are of no evolutionary importance. It would appear, therefore, that bryophytes differ strongly from pteridophytes in that interspecific hybridization is rare or absent. On the other hand, recent evidence of allopolyploid mosses (Wyatt et al. 1988, 1992, l 993a, 1993b) and liverworts (Odrzykoski, unpublished) indicates that inter­ specific hybridization does occur. Indeed, it seems likely that interspecific hybridization is common between sympatric congeners and that it simply has been overlooked in all but the most obvious (and probably least evolutionarily important) cases. Wyatt et al. ( 1992) argued that the fact that even a few hybrid sporophytes of Plagiomnium ellipticum X P. insigne managed to undergo apospory, at best a very rare process, suggests that hundreds, if not thousands, of interspecific crosses occurred. It is therefore uncertain how frequent and widespread the phenomenon of interspecific fertilization is in bryophytes. Recently, Shaw (personal communication) has detected hybridization between Mielichhoferia elongata and M. mielichhoferiana in Europe. Among liverworts, Odrzykoski and Szweykowksi ( 1991) found no evidence of crossing between the "S" and "L" sibling species of Concephalum conicum in Europe. They suggested that a prezygotic reproductive isolating mechanism is responsible for the 154 J. Hattori Bot. Lab. No. 76 I 9 9 4 complete absence of genetic recombination between these two species, which sometimes occur in mixed stands. Unfortunately, the tight coupling of ploidy level and sexuality in those groups of mosses and liverworts studied thus far makes it difficult to tease apart the independent effects of ploidy and sexuality on levels of genetic variation and its partitioning among populations. In Plagiomnium section Rosulata the highest levels of genetic variation are seen in the bisexual allopolyploid P. medium (Wyatt et al. 1992 ). Much of this apparent variation is fixed, however, because of nonsegregation of nonhomologous chromo­ somes. This is also true of the bisexual allopolyploid P. curvatulum, whose levels of genetic polymorphism are very similar to the most polymorphic of the unisexual haploid species, P. ellipticum (Wyatt et al. 1993a). In Rhizomnium section Rhizomnium levels of genetic variation overall are very low, but the highest values are again observed for populations of the bisexual allpolyploid R. pseudopunctatum (Wyatt et al. 1993b). Wyatt et al. ( 1992) have speculated that allopolyploidy provides tremendous genetic benefits to bryophytes because of their unique haploid-dominant life cycle. It allows heterozygosity to be expressed in the free-living gametophyte generation, as well as the reduced sporophyte generation. In all of the cases studied thus far, allopolyploidy allows plants to express fixed heterozygosity at loci that carry different alleles in the haploid progenitors, while it simultaneously permits recombination across loci. Thus, contrary to the view that the primary advantage of polyploidy derives from the ability of such plants to self-fertilize and have increased sporophyte production (Wyatt & Anderson 1984), it appears that the genetic benefits of polyploidy itself may be most important. Clearly, we need additional studies of bryophytes that differ in ploidy level, but not sexual condition, and that differ in sexual condition, but not ploidy level.

ACKNOWLEDGMENTS Much of the research reported here was supported by grants from the United States National Science Foundation (BSR-8408931, BSR-8806386, and DEB- 9220676). I thank my coworkers, A. Stoneburner and I. J. Odrzykoski, for their contributions to our joint research on ; G. Derda and D. Grise for laboratory assistance; a large number of bryologists who have assisted our collecting efforts and who are listed individually in relevant papers; and A. J. Shaw and I. J. Odrzykoski for allowing me to cite unpublished data. I also thank the organizers of the symposium on Reproductive Biology of Bryophytes, R. E. Longton, L. SOderstrom, and H. Deguchi, for the opportunity to speak and write about the subject of this paper.

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